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The Apicomplexa, important pathogens of humans causing diseases such as toxoplasmosis and malaria, depend on their mETC in every known stage of their complicated life cycles. Here, using a complexome profiling proteomic approach, we have characterised the\n                    <jats:italic>Toxoplasma<\/jats:italic>\n                    mETC complexes and F\n                    <jats:sub>1<\/jats:sub>\n                    F\n                    <jats:sub>o<\/jats:sub>\n                    -ATP synthase. We identified and assigned 60 proteins to complexes II, IV and F\n                    <jats:sub>1<\/jats:sub>\n                    F\n                    <jats:sub>o<\/jats:sub>\n                    -ATP synthase of\n                    <jats:italic>Toxoplasma<\/jats:italic>\n                    , of which 16 have not been identified previously. Notably, our complexome profile elucidates the composition of the\n                    <jats:italic>Toxoplasma<\/jats:italic>\n                    complex III, the target of clinically used drugs such as atovaquone. We identified two new homologous subunits and two new parasite-specific subunits, one of which is broadly conserved in myzozoans. We demonstrate all four proteins are essential for complex III stability and parasite growth, and show their depletion leads to decreased mitochondrial potential, supporting their assignment as complex III subunits. Our study highlights the divergent subunit composition of the apicomplexan mETC and F\n                    <jats:sub>1<\/jats:sub>\n                    F\n                    <jats:sub>o<\/jats:sub>\n                    -ATP synthase complexes and sets the stage for future structural and drug discovery studies.\n                  <\/jats:p>","DOI":"10.1371\/journal.ppat.1009301","type":"journal-article","created":{"date-parts":[[2021,3,2]],"date-time":"2021-03-02T13:50:35Z","timestamp":1614693035000},"page":"e1009301","update-policy":"https:\/\/doi.org\/10.1371\/journal.ppat.corrections_policy","source":"Crossref","is-referenced-by-count":88,"title":["Complexome profile of Toxoplasma gondii mitochondria identifies divergent subunits of respiratory chain complexes including new subunits of cytochrome bc1 complex"],"prefix":"10.1371","volume":"17","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-9274-9486","authenticated-orcid":true,"given":"Andrew E.","family":"Maclean","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6890-6050","authenticated-orcid":true,"given":"Hannah R.","family":"Bridges","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9034-3650","authenticated-orcid":true,"given":"Mariana F.","family":"Silva","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shujing","family":"Ding","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7522-8876","authenticated-orcid":true,"given":"Jana","family":"Ovciarikova","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8667-6797","authenticated-orcid":true,"given":"Judy","family":"Hirst","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5909-2307","authenticated-orcid":true,"given":"Lilach","family":"Sheiner","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2021,3,2]]},"reference":[{"key":"ppat.1009301.ref001","doi-asserted-by":"crossref","first-page":"18051","DOI":"10.1016\/S0021-9258(18)55235-2","article-title":"Role of an energized inner membrane in mitochondrial protein import. Delta psi drives the movement of presequences","volume":"266","author":"J Martin","year":"1991","journal-title":"J Biol Chem"},{"key":"ppat.1009301.ref002","doi-asserted-by":"crossref","first-page":"88","DOI":"10.1038\/nature05572","article-title":"Specific role of mitochondrial electron transport in blood-stage Plasmodium falciparum","volume":"446","author":"HJ Painter","year":"2007","journal-title":"Nature"},{"key":"ppat.1009301.ref003","article-title":"World Malaria Report","author":"WHO","year":"2019"},{"key":"ppat.1009301.ref004","doi-asserted-by":"crossref","first-page":"1965","DOI":"10.1016\/S0140-6736(04)16412-X","volume":"363","author":"J Montoya","year":"2004","journal-title":"Toxoplasmosis. 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Seidi","year":"2018","journal-title":"Elife"},{"key":"ppat.1009301.ref008","doi-asserted-by":"crossref","first-page":"2100","DOI":"10.1128\/AAC.44.8.2100-2108.2000","article-title":"Mutations in Plasmodium falciparum cytochrome b that are associated with atovaquone resistance are located at a putative drug-binding site","volume":"44","author":"M Korsinczky","year":"2000","journal-title":"Antimicrob Agents Chemother"},{"key":"ppat.1009301.ref009","doi-asserted-by":"crossref","first-page":"8298","DOI":"10.1073\/pnas.1205651109","article-title":"Generation of quinolone antimalarials targeting the Plasmodium falciparum mitochondrial respiratory chain for the treatment and prophylaxis of malaria","volume":"109","author":"GA Biagini","year":"2012","journal-title":"Proc Natl Acad Sci U S A"},{"key":"ppat.1009301.ref010","doi-asserted-by":"crossref","first-page":"4853","DOI":"10.1128\/AAC.00791-16","article-title":"Atovaquone and ELQ-300 combination therapy as a novel dual-site cytochrome bc1 inhibition strategy for malaria","volume":"60","author":"AM Stickles","year":"2016","journal-title":"Antimicrob Agents Chemother"},{"key":"ppat.1009301.ref011","doi-asserted-by":"crossref","first-page":"49","DOI":"10.2174\/138945007779315632","article-title":"Mitochondrial drug targets in apicomplexan parasites","volume":"8","author":"MW Mather","year":"2007","journal-title":"Curr Drug Targets"},{"key":"ppat.1009301.ref012","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1016\/j.pt.2016.10.002","article-title":"Is the Mitochondrion a Good Malaria Drug Target","volume":"33","author":"CD Goodman","year":"2017","journal-title":"Trends Parasitol"},{"key":"ppat.1009301.ref013","doi-asserted-by":"crossref","first-page":"897","DOI":"10.1016\/B978-0-12-815041-2.00020-7","volume-title":"Toxoplasma gondii","author":"D Jacot","year":"2020"},{"key":"ppat.1009301.ref014","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1093\/molbev\/mss205","article-title":"Alveolate mitochondrial metabolic evolution: Dinoflagellates force reassessment of the role of parasitism as a driver of change in apicomplexans","volume":"30","author":"JC Danne","year":"2013","journal-title":"Mol Biol Evol"},{"key":"ppat.1009301.ref015","doi-asserted-by":"crossref","first-page":"385","DOI":"10.1074\/jbc.M307264200","article-title":"Oxidative Phosphorylation and Rotenone-insensitive Malate- and NADH-Quinone Oxidoreductases in Plasmodium yoelii yoelii Mitochondria in Situ","volume":"279","author":"SA Uyemura","year":"2004","journal-title":"J Biol Chem"},{"issue":"Pt 1","key":"ppat.1009301.ref016","first-page":"17","article-title":"Mitochondria of mammalian Plasmodium spp. Parasitology","volume":"102","author":"M Fry","year":"1991"},{"key":"ppat.1009301.ref017","doi-asserted-by":"crossref","first-page":"111204","DOI":"10.1016\/j.molbiopara.2019.111204","article-title":"Same same, but different: Uncovering unique features of the mitochondrial respiratory chain of apicomplexans","volume":"232","author":"JA Hayward","year":"2019","journal-title":"Mol Biochem Parasitol"},{"key":"ppat.1009301.ref018","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1371\/journal.pbio.2006128","article-title":"Highly diverged novel subunit composition of apicomplexan F-type ATP synthase identified from Toxoplasma gondii","volume":"16","author":"R Salunke","year":"2018","journal-title":"PLoS Biol"},{"key":"ppat.1009301.ref019","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1023\/A:1005459426843","article-title":"Structure of the avian mitochondrial cytochrome bc1 complex","volume":"31","author":"EA Berry","year":"1999","journal-title":"J Bioenerg Biomembr"},{"key":"ppat.1009301.ref020","doi-asserted-by":"crossref","first-page":"2800","DOI":"10.1073\/pnas.052704699","article-title":"Crystal structure of the yeast cytochrome bc1 complex with its bound substrate cytochrome c","volume":"99","author":"C Lange","year":"2002","journal-title":"Proc Natl 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Seeber","year":"2008","journal-title":"Trends Parasitol"},{"key":"ppat.1009301.ref028","doi-asserted-by":"crossref","first-page":"152","DOI":"10.1016\/j.mib.2013.07.003","article-title":"The metabolic roles of the endosymbiotic organelles of Toxoplasma and Plasmodium spp","volume":"16","author":"L Sheiner","year":"2013","journal-title":"Curr Opin Microbiol"},{"key":"ppat.1009301.ref029","doi-asserted-by":"crossref","first-page":"e1009211","DOI":"10.1371\/journal.ppat.1009211","article-title":"Divergent features of the coenzyme Q:cytochrome c oxidoreductase complex in Toxoplasma gondii parasites","volume":"17","author":"JA Hayward","year":"2021","journal-title":"PLoS Pathog"},{"key":"ppat.1009301.ref030","doi-asserted-by":"crossref","first-page":"538","DOI":"10.1016\/j.cmet.2012.08.009","article-title":"Complexome profiling identifies TMEM126B as a component of the mitochondrial complex i assembly complex","volume":"16","author":"H Heide","year":"2012","journal-title":"Cell Metab"},{"key":"ppat.1009301.ref031","doi-asserted-by":"crossref","first-page":"128","DOI":"10.1016\/j.cmet.2016.09.002","article-title":"The Assembly Pathway of Mitochondrial Respiratory Chain Complex I","volume":"25","author":"S Guerrero-Castillo","year":"2017","journal-title":"Cell Metab"},{"key":"ppat.1009301.ref032","doi-asserted-by":"crossref","first-page":"592","DOI":"10.1016\/j.ajhg.2018.08.013","article-title":"Bi-allelic Mutations in NDUFA6 Establish Its Role in Early-Onset Isolated Mitochondrial Complex I Deficiency","volume":"103","author":"CL Alston","year":"2018","journal-title":"Am J Hum Genet"},{"key":"ppat.1009301.ref033","doi-asserted-by":"crossref","first-page":"92","DOI":"10.1016\/j.ajhg.2019.12.001","article-title":"Pathogenic Bi-allelic Mutations in NDUFAF8 Cause Leigh Syndrome with an Isolated Complex I Deficiency","volume":"106","author":"CL Alston","year":"2020","journal-title":"Am J Hum Genet"},{"key":"ppat.1009301.ref034","doi-asserted-by":"crossref","first-page":"1235","DOI":"10.1111\/mmi.14357","article-title":"Identification of the Toxoplasma gondii mitochondrial ribosome, and characterisation of a protein essential for mitochondrial translation","volume":"112","author":"A Lacombe","year":"2019","journal-title":"Mol Microbiol"},{"key":"ppat.1009301.ref035","doi-asserted-by":"crossref","first-page":"125","DOI":"10.1016\/j.mito.2006.11.021","article-title":"Mitochondria and apicoplast of Plasmodium falciparum: Behaviour on subcellular fractionation and the implication","volume":"7","author":"T Kobayashi","year":"2007","journal-title":"Mitochondrion"},{"key":"ppat.1009301.ref036","article-title":"A Comprehensive Subcellular Atlas of the Toxoplasma Proteome via hyperLOPIT Provides Spatial Context for Protein Functions","author":"K Barylyuk","year":"2020","journal-title":"Cell Host Microbe"},{"key":"ppat.1009301.ref037","doi-asserted-by":"crossref","first-page":"213","DOI":"10.1016\/j.bbadis.2005.07.003","article-title":"Proteomic analysis of succinate dehydrogenase and ubiquinol-cytochrome c reductase (Complex II and III) isolated by immunoprecipitation from bovine and mouse heart mitochondria","volume":"1762","author":"B Schilling","year":"2006","journal-title":"Biochim Biophys Acta"},{"key":"ppat.1009301.ref038","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1038\/nchem.2908","article-title":"An integrated native mass spectrometry and top-down proteomics method that connects sequence to structure and function of macromolecular complexes","volume":"10","author":"H Li","year":"2018","journal-title":"Nat Chem."},{"key":"ppat.1009301.ref039","first-page":"366","article-title":"Comment on \u201cProtein assemblies ejected directly from native membranes yield complexes for mass spectrometry\u201d","author":"J Hirst","year":"2019","journal-title":"Science"},{"key":"ppat.1009301.ref040","doi-asserted-by":"crossref","first-page":"779","DOI":"10.1111\/j.1432-1033.1996.00779.x","article-title":"Computational method to predict mitochondrially imported proteins and their targeting sequences","volume":"241","author":"MG Claros","year":"1996","journal-title":"Eur J Biochem"},{"key":"ppat.1009301.ref041","doi-asserted-by":"crossref","first-page":"120","DOI":"10.1038\/s41467-020-20381-z","article-title":"ATP synthase hexamer assemblies shape cristae of Toxoplasma mitochondria","volume":"12","author":"A M\u00fchleip","year":"2021","journal-title":"Nat Commun."},{"key":"ppat.1009301.ref042","article-title":"A novel fragmented mitochondrial genome in the protist pathogen Toxoplasma gondii and related tissue coccidia","author":"S Namasivayam","year":"2020","journal-title":"bioRxiv"},{"key":"ppat.1009301.ref043","doi-asserted-by":"crossref","first-page":"1777","DOI":"10.1093\/emboj\/19.8.1777","article-title":"Supercomplexes in the respiratory chains of yeast and mammalian mitochondria","volume":"19","author":"H Schagger","year":"2000","journal-title":"EMBO J"},{"key":"ppat.1009301.ref044","doi-asserted-by":"crossref","first-page":"1136","DOI":"10.1126\/science.272.5265.1136","article-title":"The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 A","volume":"272","author":"T Tsukihara","year":"1996","journal-title":"Science"},{"key":"ppat.1009301.ref045","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1146\/annurev.biochem.72.121801.161700","article-title":"Function and Structure of Complex II of the Respiratory Chain","volume":"72","author":"G. Cecchini","year":"2003","journal-title":"Annu Rev Biochem"},{"key":"ppat.1009301.ref046","doi-asserted-by":"crossref","DOI":"10.3390\/genes10010029","article-title":"Novel characteristics of mitochondrial electron transport chain from Eimeria tenella","volume":"10","author":"M Matsubayashi","year":"2019","journal-title":"Genes (Basel)."},{"key":"ppat.1009301.ref047","first-page":"7","article-title":"A systematic screen to discover and analyze apicoplast proteins identifies a conserved and essential protein import factor","author":"L Sheiner","year":"2011","journal-title":"PLoS Pathog"},{"key":"ppat.1009301.ref048","doi-asserted-by":"crossref","first-page":"19335","DOI":"10.1074\/jbc.M116.725069","article-title":"The import of proteins into the mitochondrion of toxoplasma gondii","volume":"291","author":"GG Van Dooren","year":"2016","journal-title":"J Biol Chem"},{"key":"ppat.1009301.ref049","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1111\/j.1365-2958.2011.07807.x","article-title":"Two internal type II NADH dehydrogenases of Toxoplasma gondii are both required for optimal tachyzoite growth","volume":"82","author":"SS Lin","year":"2011","journal-title":"Mol Microbiol"},{"key":"ppat.1009301.ref050","doi-asserted-by":"crossref","first-page":"1545","DOI":"10.1016\/0006-2952(92)90213-3","article-title":"Site of action of the antimalarial hydroxynaphthoquinone, 2-[trans-4-(4\u2019-chlorophenyl) cyclohexyl]-3- hydroxy-1,4-naphthoquinone (566C80).","volume":"43","author":"M Fry","year":"1992","journal-title":"Biochem Pharmacol"},{"key":"ppat.1009301.ref051","doi-asserted-by":"crossref","first-page":"66","DOI":"10.1016\/0169-4758(93)90040-M","article-title":"Atovaquone\u2014a novel broad-spectrum anti-infective drug","volume":"9","author":"AT Hudson","year":"1993","journal-title":"Parasitol Today"},{"key":"ppat.1009301.ref052","doi-asserted-by":"crossref","first-page":"295","DOI":"10.1016\/j.ijpddr.2018.04.007","article-title":"Functional screening of selective mitochondrial inhibitors of Plasmodium","volume":"8","author":"MG Gomez-Lorenzo","year":"2018","journal-title":"Int J Parasitol Drugs Drug Resist"},{"key":"ppat.1009301.ref053","doi-asserted-by":"crossref","first-page":"e01866","DOI":"10.1128\/AAC.01866-16","article-title":"Genetic Evidence for Cytochrome b Qi Site Inhibition by 4(1H)-Quinolone-3-Diarylethers and Antimycin in Toxoplasma gondii","volume":"61","author":"PH Alday","year":"2017","journal-title":"Antimicrob Agents Chemother"},{"key":"ppat.1009301.ref054","doi-asserted-by":"crossref","first-page":"1214","DOI":"10.1021\/cb200105d","article-title":"A chemical genomic analysis of decoquinate, a Plasmodium falciparum cytochrome b inhibitor","volume":"6","author":"TG Nam","year":"2011","journal-title":"ACS Chem Biol"},{"key":"ppat.1009301.ref055","doi-asserted-by":"crossref","first-page":"755","DOI":"10.1073\/pnas.1416611112","article-title":"Antimalarial 4(1H)-pyridones bind to the Qi site of cytochrome bc1","volume":"112","author":"MJ Capper","year":"2015","journal-title":"Proc Natl Acad Sci U S A"},{"key":"ppat.1009301.ref056","doi-asserted-by":"crossref","first-page":"1423","DOI":"10.1016\/j.cell.2016.08.019","article-title":"A Genome-wide CRISPR Screen in Toxoplasma Identifies Essential Apicomplexan Genes","volume":"166","author":"SM Sidik","year":"2016","journal-title":"Cell"},{"key":"ppat.1009301.ref057","doi-asserted-by":"crossref","first-page":"2237","DOI":"10.1016\/j.jmb.2017.12.007","article-title":"A Completely Reimplemented MPI Bioinformatics Toolkit with a New HHpred Server at its Core","volume":"430","author":"L Zimmermann","year":"2018","journal-title":"J Mol Biol"},{"key":"ppat.1009301.ref058","doi-asserted-by":"crossref","first-page":"765","DOI":"10.1016\/j.cmet.2017.03.009","article-title":"The Enigma of the Respiratory Chain Supercomplex","volume":"25","author":"D Milenkovic","year":"2017","journal-title":"Cell Metab"},{"key":"ppat.1009301.ref059","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1186\/s12915-018-0577-5","article-title":"Open questions: Respiratory chain supercomplexes-why are they there and what do they do?","volume":"16","author":"J. Hirst","year":"2018","journal-title":"BMC Biol"},{"key":"ppat.1009301.ref060","doi-asserted-by":"crossref","first-page":"31040","DOI":"10.1074\/jbc.273.47.31040","article-title":"Respiration and oxidative phosphorylation in the apicomplexan parasite Toxoplasma gondii","volume":"273","author":"AE Vercesi","year":"1998","journal-title":"J Biol Chem"},{"key":"ppat.1009301.ref061","doi-asserted-by":"crossref","first-page":"877","DOI":"10.1128\/EC.00381-08","article-title":"Type II NADH dehydrogenase inhibitor 1-hydroxy-2-dodecyl-4(1H)quinolone leads to collapse of mitochondrial inner-membrane potential and ATP depletion in Toxoplasma gondii","volume":"8","author":"SS Lin","year":"2009","journal-title":"Eukaryot Cell"},{"key":"ppat.1009301.ref062","doi-asserted-by":"crossref","first-page":"62","DOI":"10.1016\/j.chom.2009.12.002","article-title":"The Toxoplasma Apicoplast Phosphate Translocator Links Cytosolic and Apicoplast Metabolism and Is Essential for Parasite 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\u201cmatrix-targeting\u201d and the \u201csorting\u201d domains in the cytochrome c1 presequence","volume":"6","author":"AP van Loon","year":"1987","journal-title":"EMBO J"},{"key":"ppat.1009301.ref066","doi-asserted-by":"crossref","first-page":"8387","DOI":"10.1016\/S0021-9258(18)52883-0","article-title":"The mitochondrial targeting presequence of the Rieske iron-sulfur protein is processed in a single step after insertion into the cytochrome bc1 complex in mammals and retained as a subunit in the complex","volume":"268","author":"U Brandt","year":"1993","journal-title":"J Biol Chem"},{"key":"ppat.1009301.ref067","doi-asserted-by":"crossref","first-page":"229","DOI":"10.1093\/jb\/mvn161","article-title":"Mitochondrial dehydrogenases in the aerobic respiratory chain of the rodent malaria parasite Plasmodium yoelii yoelii","volume":"145","author":"K Kawahara","year":"2009","journal-title":"J Biochem"},{"key":"ppat.1009301.ref068","doi-asserted-by":"crossref","first-page":"443","DOI":"10.1016\/j.mito.2009.08.004","article-title":"Identification of mitochondrial Complex II subunits SDH3 and SDH4 and ATP synthase subunits a and b in Plasmodium spp","volume":"9","author":"T Mogi","year":"2009","journal-title":"Mitochondrion"},{"key":"ppat.1009301.ref069","article-title":"Composition and stage dynamics of mitochondrial complexes in Plasmodium falciparum","author":"F Evers","year":"2020","journal-title":"bioRxiv."},{"key":"ppat.1009301.ref070","doi-asserted-by":"crossref","first-page":"440","DOI":"10.1016\/j.cbpa.2010.05.005","article-title":"Inhibiting Plasmodium cytochrome bc1: A complex issue","volume":"14","author":"V Barton","year":"2010","journal-title":"Curr Opin Chem Biol"},{"key":"ppat.1009301.ref071","doi-asserted-by":"crossref","first-page":"183","DOI":"10.1111\/j.1567-1364.2007.00328.x","article-title":"Molecular basis of resistance to cytochrome bc1 inhibitors","volume":"8","author":"N Fisher","year":"2008","journal-title":"FEMS Yeast Res"},{"key":"ppat.1009301.ref072","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/ncomms5029","article-title":"Structural analysis of atovaquone-inhibited cytochrome bc 1 complex reveals the molecular basis of antimalarial drug action","volume":"5","author":"D Birth","year":"2014","journal-title":"Nat Commun"},{"key":"ppat.1009301.ref073","doi-asserted-by":"crossref","first-page":"15936","DOI":"10.1073\/pnas.1208069109","article-title":"Endochin-like quinolones are highly efficacious against acute and latent experimental toxoplasmosis","volume":"109","author":"JS Doggett","year":"2012","journal-title":"Proc Natl Acad Sci U S A"},{"key":"ppat.1009301.ref074","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1038\/s41594-018-0169-7","article-title":"Cryo-EM structure of the yeast respiratory supercomplex","volume":"26","author":"S Rathore","year":"2019","journal-title":"Nat Struct 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of endogenous genes in a Toxoplasma gondii strain lacking Ku80","volume":"8","author":"MH Huynh","year":"2009","journal-title":"Eukaryot Cell"},{"key":"ppat.1009301.ref079","doi-asserted-by":"crossref","first-page":"13574","DOI":"10.1073\/pnas.0803862105","article-title":"Toxoplasma gondii Tic20 is essential for apicoplast protein import","volume":"105","author":"GG van Dooren","year":"2008","journal-title":"Proc Natl Acad Sci U S A"},{"key":"ppat.1009301.ref080","doi-asserted-by":"crossref","first-page":"402","DOI":"10.1006\/meth.2001.1262","article-title":"Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method","volume":"25","author":"KJ Livak","year":"2001","journal-title":"Methods"},{"key":"ppat.1009301.ref081","doi-asserted-by":"crossref","first-page":"682","DOI":"10.1016\/j.chom.2012.09.013","article-title":"Mitochondrial metabolism of glucose and glutamine is required for intracellular growth of toxoplasma gondii","volume":"12","author":"JI MacRae","year":"2012","journal-title":"Cell Host Microbe"},{"key":"ppat.1009301.ref082","doi-asserted-by":"crossref","first-page":"4353","DOI":"10.1128\/IAI.70.8.4353-4361.2002","article-title":"Clostridium septicum alpha-toxin is active against the parasitic protozoan Toxoplasma gondii and targets members of the SAG family of glycosylphosphatidylinositol-anchored surface proteins","volume":"70","author":"MJ Wichroski","year":"2002","journal-title":"Infect Immun"},{"key":"ppat.1009301.ref083","doi-asserted-by":"crossref","first-page":"33683","DOI":"10.1074\/jbc.M109.044024","article-title":"Genetic evidence that an endosymbiont-derived endoplasmic reticulum-associated protein degradation (ERAD) system functions in import of apicoplast proteins","volume":"284","author":"S Agrawal","year":"2009","journal-title":"J Biol Chem"},{"key":"ppat.1009301.ref084","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/srep42746","article-title":"Mitochondrial behaviour throughout the lytic cycle of Toxoplasma gondii","volume":"7","author":"J Ovciarikova","year":"2017","journal-title":"Sci Rep"},{"key":"ppat.1009301.ref085","doi-asserted-by":"crossref","first-page":"125","DOI":"10.1007\/978-1-59745-365-3_9","article-title":"Isolation of intact, functional mitochondria from the model plant Arabidopsis thaliana","volume":"372","author":"LJ Sweetlove","year":"2007","journal-title":"Methods Mol Biol"},{"key":"ppat.1009301.ref086","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1016\/j.bbabio.2016.12.001","article-title":"Subunit NDUFV3 is present in two distinct isoforms in mammalian complex I","volume":"1858","author":"HR Bridges","year":"2017","journal-title":"Biochim Biophys Acta 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